Two genomes of highly polyphagous lepidopteran pests (Spodoptera frugiperda, Noctuidae) with different host-plant ranges

Anaïs Gouin, Anthony Bretaudeau, Kiwoong Nam, Sylvie Gimenez, Jean Marc Aury, Bernard Duvic, Frédérique Hilliou, Nicolas Durand, Nicolas Montagné, Isabelle Darboux, Suyog Kuwar, Thomas Chertemps, David Siaussat, Anne Bretschneider, Yves Moné, Seung Joon Ahn, Sabine Hänniger, Anne Sophie Gosselin Grenet, David Neunemann, Florian Maumus & 45 others Isabelle Luyten, Karine Labadie, Wei Xu, Fotini Koutroumpa, Jean Michel Escoubas, Angel Llopis, Martine Maïbèche-Coisne, Fanny Salasc, Archana Tomar, Alisha R. Anderson, Sher Afzal Khan, Pascaline Dumas, Marion Orsucci, Julie Guy, Caroline Belser, Adriana Alberti, Benjamin Noel, Arnaud Couloux, Jonathan Mercier, Sabine Nidelet, Emeric Dubois, Nai Yong Liu, Isabelle Boulogne, Olivier Mirabeau, Gaelle Le Goff, Karl Gordon, John Oakeshott, Fernando L. Consoli, Anne Nathalie Volkoff, Howard William Fescemyer, James Harold Marden, Dawn S. Luthe, Salvador Herrero, David G. Heckel, Patrick Wincker, Gael J. Kergoat, Joelle Amselem, Hadi Quesneville, Astrid T. Groot, Emmanuelle Jacquin-Joly, Nicolas Nègre, Claire Lemaitre, Fabrice Legeai, Emmanuelle D'Alençon, Philippe Fournier

Research output: Contribution to journalArticle

33 Citations (Scopus)

Abstract

Emergence of polyphagous herbivorous insects entails significant adaptation to recognize, detoxify and digest a variety of host-plants. Despite of its biological and practical importance - since insects eat 20% of crops - no exhaustive analysis of gene repertoires required for adaptations in generalist insect herbivores has previously been performed. The noctuid moth Spodoptera frugiperda ranks as one of the world's worst agricultural pests. This insect is polyphagous while the majority of other lepidopteran herbivores are specialist. It consists of two morphologically indistinguishable strains ("C" and "R") that have different host plant ranges. To describe the evolutionary mechanisms that both enable the emergence of polyphagous herbivory and lead to the shift in the host preference, we analyzed whole genome sequences from laboratory and natural populations of both strains. We observed huge expansions of genes associated with chemosensation and detoxification compared with specialist Lepidoptera. These expansions are largely due to tandem duplication, a possible adaptation mechanism enabling polyphagy. Individuals from natural C and R populations show significant genomic differentiation. We found signatures of positive selection in genes involved in chemoreception, detoxification and digestion, and copy number variation in the two latter gene families, suggesting an adaptive role for structural variation.

Original languageEnglish (US)
Article number11816
JournalScientific reports
Volume7
Issue number1
DOIs
StatePublished - Dec 1 2017

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Spodoptera
Host Specificity
Herbivory
Insects
Genome
Genes
Lepidoptera
Moths
Population
Digestion

All Science Journal Classification (ASJC) codes

  • General

Cite this

Gouin, Anaïs ; Bretaudeau, Anthony ; Nam, Kiwoong ; Gimenez, Sylvie ; Aury, Jean Marc ; Duvic, Bernard ; Hilliou, Frédérique ; Durand, Nicolas ; Montagné, Nicolas ; Darboux, Isabelle ; Kuwar, Suyog ; Chertemps, Thomas ; Siaussat, David ; Bretschneider, Anne ; Moné, Yves ; Ahn, Seung Joon ; Hänniger, Sabine ; Grenet, Anne Sophie Gosselin ; Neunemann, David ; Maumus, Florian ; Luyten, Isabelle ; Labadie, Karine ; Xu, Wei ; Koutroumpa, Fotini ; Escoubas, Jean Michel ; Llopis, Angel ; Maïbèche-Coisne, Martine ; Salasc, Fanny ; Tomar, Archana ; Anderson, Alisha R. ; Khan, Sher Afzal ; Dumas, Pascaline ; Orsucci, Marion ; Guy, Julie ; Belser, Caroline ; Alberti, Adriana ; Noel, Benjamin ; Couloux, Arnaud ; Mercier, Jonathan ; Nidelet, Sabine ; Dubois, Emeric ; Liu, Nai Yong ; Boulogne, Isabelle ; Mirabeau, Olivier ; Le Goff, Gaelle ; Gordon, Karl ; Oakeshott, John ; Consoli, Fernando L. ; Volkoff, Anne Nathalie ; Fescemyer, Howard William ; Marden, James Harold ; Luthe, Dawn S. ; Herrero, Salvador ; Heckel, David G. ; Wincker, Patrick ; Kergoat, Gael J. ; Amselem, Joelle ; Quesneville, Hadi ; Groot, Astrid T. ; Jacquin-Joly, Emmanuelle ; Nègre, Nicolas ; Lemaitre, Claire ; Legeai, Fabrice ; D'Alençon, Emmanuelle ; Fournier, Philippe. / Two genomes of highly polyphagous lepidopteran pests (Spodoptera frugiperda, Noctuidae) with different host-plant ranges. In: Scientific reports. 2017 ; Vol. 7, No. 1.
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Gouin, A, Bretaudeau, A, Nam, K, Gimenez, S, Aury, JM, Duvic, B, Hilliou, F, Durand, N, Montagné, N, Darboux, I, Kuwar, S, Chertemps, T, Siaussat, D, Bretschneider, A, Moné, Y, Ahn, SJ, Hänniger, S, Grenet, ASG, Neunemann, D, Maumus, F, Luyten, I, Labadie, K, Xu, W, Koutroumpa, F, Escoubas, JM, Llopis, A, Maïbèche-Coisne, M, Salasc, F, Tomar, A, Anderson, AR, Khan, SA, Dumas, P, Orsucci, M, Guy, J, Belser, C, Alberti, A, Noel, B, Couloux, A, Mercier, J, Nidelet, S, Dubois, E, Liu, NY, Boulogne, I, Mirabeau, O, Le Goff, G, Gordon, K, Oakeshott, J, Consoli, FL, Volkoff, AN, Fescemyer, HW, Marden, JH, Luthe, DS, Herrero, S, Heckel, DG, Wincker, P, Kergoat, GJ, Amselem, J, Quesneville, H, Groot, AT, Jacquin-Joly, E, Nègre, N, Lemaitre, C, Legeai, F, D'Alençon, E & Fournier, P 2017, 'Two genomes of highly polyphagous lepidopteran pests (Spodoptera frugiperda, Noctuidae) with different host-plant ranges', Scientific reports, vol. 7, no. 1, 11816. https://doi.org/10.1038/s41598-017-10461-4

Two genomes of highly polyphagous lepidopteran pests (Spodoptera frugiperda, Noctuidae) with different host-plant ranges. / Gouin, Anaïs; Bretaudeau, Anthony; Nam, Kiwoong; Gimenez, Sylvie; Aury, Jean Marc; Duvic, Bernard; Hilliou, Frédérique; Durand, Nicolas; Montagné, Nicolas; Darboux, Isabelle; Kuwar, Suyog; Chertemps, Thomas; Siaussat, David; Bretschneider, Anne; Moné, Yves; Ahn, Seung Joon; Hänniger, Sabine; Grenet, Anne Sophie Gosselin; Neunemann, David; Maumus, Florian; Luyten, Isabelle; Labadie, Karine; Xu, Wei; Koutroumpa, Fotini; Escoubas, Jean Michel; Llopis, Angel; Maïbèche-Coisne, Martine; Salasc, Fanny; Tomar, Archana; Anderson, Alisha R.; Khan, Sher Afzal; Dumas, Pascaline; Orsucci, Marion; Guy, Julie; Belser, Caroline; Alberti, Adriana; Noel, Benjamin; Couloux, Arnaud; Mercier, Jonathan; Nidelet, Sabine; Dubois, Emeric; Liu, Nai Yong; Boulogne, Isabelle; Mirabeau, Olivier; Le Goff, Gaelle; Gordon, Karl; Oakeshott, John; Consoli, Fernando L.; Volkoff, Anne Nathalie; Fescemyer, Howard William; Marden, James Harold; Luthe, Dawn S.; Herrero, Salvador; Heckel, David G.; Wincker, Patrick; Kergoat, Gael J.; Amselem, Joelle; Quesneville, Hadi; Groot, Astrid T.; Jacquin-Joly, Emmanuelle; Nègre, Nicolas; Lemaitre, Claire; Legeai, Fabrice; D'Alençon, Emmanuelle; Fournier, Philippe.

In: Scientific reports, Vol. 7, No. 1, 11816, 01.12.2017.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Two genomes of highly polyphagous lepidopteran pests (Spodoptera frugiperda, Noctuidae) with different host-plant ranges

AU - Gouin, Anaïs

AU - Bretaudeau, Anthony

AU - Nam, Kiwoong

AU - Gimenez, Sylvie

AU - Aury, Jean Marc

AU - Duvic, Bernard

AU - Hilliou, Frédérique

AU - Durand, Nicolas

AU - Montagné, Nicolas

AU - Darboux, Isabelle

AU - Kuwar, Suyog

AU - Chertemps, Thomas

AU - Siaussat, David

AU - Bretschneider, Anne

AU - Moné, Yves

AU - Ahn, Seung Joon

AU - Hänniger, Sabine

AU - Grenet, Anne Sophie Gosselin

AU - Neunemann, David

AU - Maumus, Florian

AU - Luyten, Isabelle

AU - Labadie, Karine

AU - Xu, Wei

AU - Koutroumpa, Fotini

AU - Escoubas, Jean Michel

AU - Llopis, Angel

AU - Maïbèche-Coisne, Martine

AU - Salasc, Fanny

AU - Tomar, Archana

AU - Anderson, Alisha R.

AU - Khan, Sher Afzal

AU - Dumas, Pascaline

AU - Orsucci, Marion

AU - Guy, Julie

AU - Belser, Caroline

AU - Alberti, Adriana

AU - Noel, Benjamin

AU - Couloux, Arnaud

AU - Mercier, Jonathan

AU - Nidelet, Sabine

AU - Dubois, Emeric

AU - Liu, Nai Yong

AU - Boulogne, Isabelle

AU - Mirabeau, Olivier

AU - Le Goff, Gaelle

AU - Gordon, Karl

AU - Oakeshott, John

AU - Consoli, Fernando L.

AU - Volkoff, Anne Nathalie

AU - Fescemyer, Howard William

AU - Marden, James Harold

AU - Luthe, Dawn S.

AU - Herrero, Salvador

AU - Heckel, David G.

AU - Wincker, Patrick

AU - Kergoat, Gael J.

AU - Amselem, Joelle

AU - Quesneville, Hadi

AU - Groot, Astrid T.

AU - Jacquin-Joly, Emmanuelle

AU - Nègre, Nicolas

AU - Lemaitre, Claire

AU - Legeai, Fabrice

AU - D'Alençon, Emmanuelle

AU - Fournier, Philippe

PY - 2017/12/1

Y1 - 2017/12/1

N2 - Emergence of polyphagous herbivorous insects entails significant adaptation to recognize, detoxify and digest a variety of host-plants. Despite of its biological and practical importance - since insects eat 20% of crops - no exhaustive analysis of gene repertoires required for adaptations in generalist insect herbivores has previously been performed. The noctuid moth Spodoptera frugiperda ranks as one of the world's worst agricultural pests. This insect is polyphagous while the majority of other lepidopteran herbivores are specialist. It consists of two morphologically indistinguishable strains ("C" and "R") that have different host plant ranges. To describe the evolutionary mechanisms that both enable the emergence of polyphagous herbivory and lead to the shift in the host preference, we analyzed whole genome sequences from laboratory and natural populations of both strains. We observed huge expansions of genes associated with chemosensation and detoxification compared with specialist Lepidoptera. These expansions are largely due to tandem duplication, a possible adaptation mechanism enabling polyphagy. Individuals from natural C and R populations show significant genomic differentiation. We found signatures of positive selection in genes involved in chemoreception, detoxification and digestion, and copy number variation in the two latter gene families, suggesting an adaptive role for structural variation.

AB - Emergence of polyphagous herbivorous insects entails significant adaptation to recognize, detoxify and digest a variety of host-plants. Despite of its biological and practical importance - since insects eat 20% of crops - no exhaustive analysis of gene repertoires required for adaptations in generalist insect herbivores has previously been performed. The noctuid moth Spodoptera frugiperda ranks as one of the world's worst agricultural pests. This insect is polyphagous while the majority of other lepidopteran herbivores are specialist. It consists of two morphologically indistinguishable strains ("C" and "R") that have different host plant ranges. To describe the evolutionary mechanisms that both enable the emergence of polyphagous herbivory and lead to the shift in the host preference, we analyzed whole genome sequences from laboratory and natural populations of both strains. We observed huge expansions of genes associated with chemosensation and detoxification compared with specialist Lepidoptera. These expansions are largely due to tandem duplication, a possible adaptation mechanism enabling polyphagy. Individuals from natural C and R populations show significant genomic differentiation. We found signatures of positive selection in genes involved in chemoreception, detoxification and digestion, and copy number variation in the two latter gene families, suggesting an adaptive role for structural variation.

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U2 - 10.1038/s41598-017-10461-4

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JF - Scientific Reports

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